Claire A. McLean

Geographic variation in animal colour polymorphisms and its role in speciation

Polymorphic species, in which multiple variants coexist within a population, are often used as model systems in evolutionary biology. Recent research has been dominated by the hypothesis that polymorphism can be a precursor to speciation. To date, the majority of research regarding polymorphism and speciation has focused on whether polymorphism is maintained within a population or whether morphs within populations may diverge to form separate species (sympatric speciation); however, the geographical context of speciation in polymorphic systems is likely to be both diverse and complex. In this review, we draw attention to the geographic variation in morph composition and frequencies that characterises many, if not most polymorphic species. Recent theoretical and empirical developments suggest that such variation in the number, type and frequency of morphs present among populations can increase the probability of speciation. Thus, the geographical context of a polymorphism requires a greater research focus. Here, we review the prevalence, causes and evolutionary consequences of geographic variation in polymorphism in colour‐polymorphic animal species. The prevalence and nature of geographic variation in polymorphism suggests that polymorphism may be a precursor to and facilitate speciation more commonly than appreciated previously. We argue that a better understanding of the processes generating geographic variation in polymorphism is vital to understanding how polymorphism can promote speciation.

Local adaptation and divergence in colour signal conspicuousness between monomorphic and polymorphic lineages in a lizard

Population differences in visual environment can lead to divergence in multiple components of animal coloration including signalling traits and colour patterns important for camouflage. Divergence may reflect selection imposed by different receivers (conspecifics, predators), which depends in turn on the location of the colour patch. We tested for local adaptation of two genetically and phenotypically divergent lineages of a rock‐inhabiting lizard, Ctenophorus decresii, by comparing the visual contrast of colour patches to different receivers in native and non‐native environments. The lineages differ most notably in male throat coloration, which is polymorphic in the northern lineage and monomorphic in the southern lineage, but also differ in dorsal and lateral coloration, which is visible to both conspecifics and potential predators. Using models of animal colour vision, we assessed whether lineage‐specific throat, dorsal and lateral coloration enhanced conspicuousness to conspecifics, increased crypsis to birds or both, respectively, when viewed against the predominant backgrounds from each lineage. Throat colours were no more conspicuous against native than non‐native rock but contrasted more strongly with native lichen, which occurs patchily on rocks inhabited by C. decresii. Conversely, neck coloration (lateral) more closely matched native lichen. Furthermore, although dorsal coloration of southern males was consistently more conspicuous to birds than that of northern males, both lineages had similar absolute conspicuousness against their native backgrounds. Combined, our results are consistent with local adaptation of multiple colour traits in relation to multiple receivers, suggesting that geographic variation in background colour has influenced the evolution of lineage‐specific coloration in C. decresii.

Spectral sensitivity of cone photoreceptors and opsin expression in two colour-divergent lineages of the lizard Ctenophorus decresii.

ABSTRACT Intraspecific differences in sensory perception are rarely reported but may occur when a species range extends across varying sensory environments, or there is coevolution between the sensory system and a varying signal. Examples in colour vision and colour signals are rare in terrestrial systems. The tawny dragon lizard Ctenophorus decresii is a promising candidate for such intraspecific variation, because the species comprises two geographically and genetically distinct lineages in which throat colour (a social signal used in intra- and inter-specific interactions) is locally adapted to the habitat and differs between lineages. Male lizards from the southern lineage have UV-blue throats, whereas males from the northern lineage are polymorphic with four discrete throat colours that all show minimal UV reflectance. Here, we determine the cone photoreceptor spectral sensitivities and opsin expression of the two lineages, to test whether they differ, particularly in the UV wavelengths. Using microspectrophotometry on retinal cone photoreceptors, we identified a long-wavelength-sensitive (LWS) visual pigment, a ‘short’ and ‘long’ medium-wavelength-sensitive (MWS) pigment and a short-wavelength-sensitive (SWS) pigment, all of which did not differ in λmax between lineages. Through transcriptome analysis of opsin genes we found that both lineages express four cone opsin genes, including the SWS1 opsin with peak sensitivity in the UV range, and that amino acid sequences did not differ between lineages with the exception of a single leucine to valine substitution in the RH2 opsin. Counts of yellow and transparent oil droplets associated with LWS+MWS and SWS+UVS cones, respectively, showed no difference in relative cone proportions between lineages. Therefore, contrary to predictions, we find no evidence of differences between lineages in single cone photoreceptor spectral sensitivity or opsin expression. However, we confirm the presence of four single cone classes, suggesting tetrachromacy in C. decresii, and we also provide the first evidence of UV sensitivity in agamid lizards. Summary: Microspectrophotometry and opsin expression reveals four single cone classes without intraspecific differentiation, providing the first evidence of UV sensitivity in agamid lizards.

The genetic basis of discrete and quantitative colour variation in the polymorphic lizard, Ctenophorus decresii

BackgroundColour polymorphic species provide invaluable insight into processes that generate and maintain intra-specific variation. Despite an increasing understanding of the genetic basis of discrete morphs, sources of colour variation within morphs remain poorly understood. Here we use the polymorphic tawny dragon lizard Ctenophorus decresii to test simple Mendelian models for the inheritance of discrete morphs, and to investigate the genetic basis of continuous variation among individuals across morphs. Males of this species express either orange, yellow, orange surrounded by yellow, or grey throats. Although four discrete morphs are recognised, the extent of orange and yellow varies greatly. We artificially elevated testosterone in F0 females and F1 juveniles to induce them to express the male throat colour polymorphism, and quantified colour variation across the pedigree.ResultsInheritance of discrete morphs in C. decresii best fit a model whereby two autosomal loci with complete dominance respectively determine the presence of orange and yellow. However, a single locus model with three co-dominant alleles for orange, yellow and grey could not be definitively rejected. Additionally, quantitative expression of the proportion of orange and yellow on the throat was strongly heritable (orange: h2 = 0.84 ± 0.14; yellow: h2 = 0.67 ± 0.19), with some evidence for covariance between the two.ConclusionsOur study supports the theoretical prediction that polymorphism should be governed by few genes of major effect, but implies broader genetic influence on variation in constituent morph traits.

Rival assessment and comparison of morphological and performance-based predictors of fighting ability in Lake Eyre dragon lizards, Ctenophorus maculosus

Although the outcome of contests is often critical to fitness, we still have much to learn regarding the reliability of different predictors of fighting ability (e.g. morphological traits versus performance measures) and the strategies individuals use to decide when to withdraw. We examined predictors of contest success and assessment strategies in staged contests between male Lake Eyre dragon lizards, Ctenophorus maculosus, in which males engage in escalated contests. Bite force was the only significant predictor of contest success. Although head width and depth predicted the number and duration of bites during contests, neither of these traits predicted contest outcome, nor did body size or experience in the prior two contests. These results support the view that measures of physical performance may be more reliable indicators of male fighting ability in escalated contests than morphological traits, because performance is more directly linked to the quality being signalled (i.e. fighting ability). Contest intensity was positively associated with the resource holding potential (RHP) of the loser, but not that of the winner or RHP asymmetry, indicating that individuals base their decision to withdraw on assessment of their own cost threshold (self-assessment) rather than assessment of their opponent’s ability (mutual assessment). Lastly, the number of displays (head bobs and push-ups) was also correlated with the RHP of losers (but not winners or RHP asymmetry), consistent with the recently proposed ‘information conflict hypothesis’, which predicts that weaker individuals should limit information transfer about their ability by performing fewer displays.

Do female Lake Eyre dragon lizards adjust courtship rejection behaviour under higher predation risk

Female resistance is expected to evolve when mating costs outweigh resistance costs. One potential cost of resistance is increased predation risk; however, the ability to compensate behaviourally may reduce these costs. In the Lake Eyre dragon, Ctenophorus maculosus , non-receptive females employ several rejection strategies, including lateral threat displays and flipping over, to prevent superfluous matings. C. maculosus rely on cryptic dorsal colouration for protection from predators; however, resisting females are highly conspicuous as they develop orange ventro-lateral colouration, which is emphasised during rejection displays. Furthermore, flipping over may increase vulnerability to predators by decreasing a females ability to detect predators and to flee. We tested whether females behaviourally compensate for potential increased vulnerability by altering their use of lateral threats and flip-overs under high and low perceived predation risk. The duration of flip-over rejections was significantly lower under high predation but there was no effect of predation risk on the frequency or duration of lateral threats. This suggests that females may compensate for reduced mobility or ability to detect predators rather than increased conspicuousness. Our study confirms that females are able to modulate resistance behaviour in relation to predation risk, potentially altering the trade-off between mating costs and costs of resistance.

Revealing the Biochemical and Genetic Basis of Color Variation in a Polymorphic Lizard

Determining the mechanistic and genetic basis of animal coloration is essential to understand the costs and constraints on color production, and the evolution and maintenance of phenotypic variation. However, genes underlying structural color and widespread pigment classes apart from melanin remain largely uncharacterized, in part due to restricted taxonomic focus. We combined liquid chromatography-mass spectrometry and RNA-seq gene expression analyses to characterize the pigments and genes associated with skin color in the polymorphic lizard, Ctenophorus decresii. Throat coloration in male C. decresii may be a combination of orange, yellow, grey, or ultra-violet blue. We confirmed the presence of two biochemically different pigment classes, pteridines (self-synthesized) and carotenoids (acquired through the diet), in all skin colors. Orange skin had the highest levels of pteridine pigments while yellow skin tended to have higher levels of carotenoids, of which the vitamin A precursors β-carotene and β-cryptoxanthin have not been previously confirmed in reptiles. These results were confirmed by gene expression analyses, which detected 489 genes differentially expressed between the skin colors, including genes associated with pteridine production, provitamin A carotenoid metabolism, iridophore-specific synthesis, melanin synthesis, and steroid hormone pathways. For the majority of these 489 genes, however, our study reveals a new association with color production in vertebrates. These data represent a significant contribution to understanding the genetic basis of color variation in vertebrates and a rich resource for further studies.